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Characterization of the trunk neural crest in the bamboo shark, Chiloscyllium punctatum

Juarez, Marilyn and Reyes, Michelle and Coleman, Tiffany and Rotenstein, Lisa and Sao, Sothy and Martinez, Darwin and Jones, Matthew and Mackelprang, Rachel and De Bellard, Maria Elena (2013) Characterization of the trunk neural crest in the bamboo shark, Chiloscyllium punctatum. Journal of Comparative Neurology, 521 (14). pp. 3303-3320. ISSN 0021-9967. PMCID PMC3729875. doi:10.1002/cne.23351. https://resolver.caltech.edu/CaltechAUTHORS:20130830-143744531

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Abstract

The neural crest is a population of mesenchymal cells that after migrating from the neural tube gives rise to structure and cell types: the jaw, part of the peripheral ganglia, and melanocytes. Although much is known about neural crest development in jawed vertebrates, a clear picture of trunk neural crest development for elasmobranchs is yet to be developed. Here we present a detailed study of trunk neural crest development in the bamboo shark, Chiloscyllium punctatum. Vital labeling with dioctadecyl tetramethylindocarbocyanine perchlorate (DiI) and in situ hybridization using cloned Sox8 and Sox9 probes demonstrated that trunk neural crest cells follow a pattern similar to the migratory paths already described in zebrafish and amphibians. We found shark trunk neural crest along the rostral side of the somites, the ventromedial pathway, the branchial arches, the gut, the sensory ganglia, and the nerves. Interestingly, C. punctatum Sox8 and Sox9 sequences aligned with vertebrate SoxE genes, but appeared to be more ancient than the corresponding vertebrate paralogs. The expression of these two SoxE genes in trunk neural crest cells, especially Sox9, matched the Sox10 migratory patterns observed in teleosts. Also of interest, we observed DiI cells and Sox9 labeling along the lateral line, suggesting that in C. punctatum, glial cells in the lateral line are likely of neural crest origin. Although this has been observed in other vertebrates, we are the first to show that the pattern is present in cartilaginous fishes. These findings demonstrate that trunk neural crest cell development in C. punctatum follows the same highly conserved migratory pattern observed in jawed vertebrates.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1002/cne.23351 DOIArticle
http://onlinelibrary.wiley.com/doi/10.1002/cne.23351/abstractPublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3729875/PubMed CentralArticle
Additional Information:© 2013 Wiley Periodicals, Inc. Received November 12, 2012; Revised April 15, 2013; Accepted for publication April 25, 2013. Article first published online: 25 Jul. 2013. The first three authors contributed equally to this work. Grant sponsor: National Institute of Neurological Disorders and Stroke, National Institutes of Health; Grant numbers: 2R15NS060099-02A1 and 5SC3GM096904-02 (to M.E.dB.); Grant sponsor: National Institutes of Health; Grant number: GM 2 T34 GM008959 (to M.E. Zavala for support for M.J.). We give special thanks to Chris Plante and Michelle Malme from the Long Beach Aquarium for providing us the shark embryos; to John Reiss for his helpful comments; and to Kent Coleman for his valuable revisions to this manuscript. Role of Authors: All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. MJ: performed in situ hybridizations; MR: performed DiI injections; TC: performed DNA/protein analyses, designed phylogenetic figures, performed bioinformatics analysis, and revised the manuscript; LR: performed SEM; SS: performed sectioning; DM and MJ: performed Sox8 and Sox9 cloning; RM: oversaw bioinformatics analysis; MEdB: wrote the manuscript, and performed Sox8 and Sox9 cloning and DiI injections.
Funders:
Funding AgencyGrant Number
National Institute of Neurological Disorders and Stroke (NINDS)UNSPECIFIED
NIH2R15NS060099-02A1
NIH5SC3GM096904-02
NIH Predoctoral FellowshipGM 2 T34 GM008959
Subject Keywords:shark embryo; sox8; sox9; neural crest; Chiloscyllium punctatum
Issue or Number:14
PubMed Central ID:PMC3729875
DOI:10.1002/cne.23351
Record Number:CaltechAUTHORS:20130830-143744531
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20130830-143744531
Official Citation:Juarez, M., Reyes, M., Coleman, T., Rotenstein, L., Sao, S., Martinez, D., Jones, M., Mackelprang, R. and De Bellard, M. E. (2013), Characterization of the trunk neural crest in the bamboo shark, Chiloscyllium punctatum. J. Comp. Neurol., 521: 3303–3320. doi: 10.1002/cne.23351
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:41040
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:11 Sep 2013 21:58
Last Modified:10 Nov 2021 04:25

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